Olfactory Mating Signals in the Migratory Locust Locusta migratoria.

Swarming locusts cause huge plagues across the world threatening food production. Before swarms form, locust populations exhibit a dramatic phase change from a solitary to a gregarious phase. The cause of this phase change is a complicated interplay of conspecific and environmental cues and is, especially for one of the major pests, the migratory locust Locusta migratoria, still not well understood. Here we study the behavior of both solitary and gregarious L. migratoria towards the headspace odors of conspecifics. As we do not find a general attraction of gregarious animals to the headspace of gregarious conspecifics, swarm formation does not seem to be mainly governed by olfactory aggregation cues. When testing for potential mating signals, we observe that the headspace of virgin gregarious females is highly attractive only towards virgin males of the same phase, while mated gregarious males and solitary males, regardless of their mating state, do not become attracted. Interestingly, this phase-specific attraction goes along with the finding, that mating behavior in experiments with inter-phasic pairings is extremely rare. Our data suggest that odor emissions in L. migratoria play a significant role in a mating context.

Carbonyl products of ozone oxidation of volatile organic compounds can modulate olfactory choice behavior in insects.

Insects are a diverse group of organisms that provide important ecosystem services like pollination, pest control, and decomposition and rely on olfaction to perform these services. In the Anthropocene, increasing concentrations of oxidant pollutants such as ozone have been shown to corrupt odor-driven behavior in insects by chemically degrading e.g. flower signals or insect pheromones. The degradation, however, does not only result in a loss of signals, but also in a potential enrichment of oxidation products, predominantly small carbonyls. Whether and how these oxidation products affect insect olfactory perception remains unclear. We examined the effects of ozone-generated small carbonyls on the olfactory behavior of the vinegar fly Drosophila melanogaster. We compiled a broad collection of neurophysiologically relevant odorants for the fly from databases and literature and predicted the formation of the types of stable small carbonyl products resulting from the odorant's oxidation by ozone. Based on these predictions, we evaluated the olfactory detection and behavioral impact of the ten most frequently predicted carbonyl products in the fly using single sensillum recordings (SSRs) and behavioral tests. Our results demonstrate that the fly's olfactory system can detect the oxidation products, which then elicit either attractive or neutral behavioral responses, rather than repulsion. However, certain products alter behavioral choices to an attractive odor source of balsamic vinegar. Our findings suggest that the enrichment of small carbonyl oxidation products due to increased ozone levels can affect olfactory guided insect behavior. Our study underscores the implications for odor-guided foraging in insects and the essential ecosystem services they offer under carbonyl enriched environments.

Odorant detection in a locust exhibits unusually low redundancy.

Olfactory coding, from insects to humans, is canonically considered to involve considerable across-fiber coding already at the peripheral level, thereby allowing recognition of vast numbers of odor compounds. We show that the migratory locust has evolved an alternative strategy built on highly specific odorant receptors feeding into a complex primary processing center in the brain. By collecting odors from food and different life stages of the locust, we identified 205 ecologically relevant odorants, which we used to deorphanize 48 locust olfactory receptors via ectopic expression in Drosophila. Contrary to the often broadly tuned olfactory receptors of other insects, almost all locust receptors were found to be narrowly tuned to one or very few ligands. Knocking out a single receptor using CRISPR abolished physiological and behavioral responses to the corresponding ligand. We conclude that the locust olfactory system, with most olfactory receptors being narrowly tuned, differs from the so-far described olfactory systems.